cortex 113 (2019) 210e228 Available online at www.sciencedirect.com ScienceDirect Journal homepage: www.elsevier.com/locate/cortex Research Report Beta oscillations precede joint attention and correlate with mentalization in typical development and autism * Patricia Soto-Icaza a, , Lorena Vargas c, Francisco Aboitiz a and ** Pablo Billeke b, a Laboratorio de Neurociencias Cognitivas, Departamento de Psiquiatrı´a, Centro Interdisciplinario de Neurociencias, Facultad de Medicina, Pontificia Universidad Catolica de Chile, Santiago, Chile b Division de Neurociencias, Centro de Investigacion en Complejidad Social (neuroCICS), Facultad de Gobierno, Universidad del Desarrollo, Santiago, Chile c Hospital Luis Calvo Mackenna, Santiago, Chile article info abstract Article history: A precursor of adult social functioning is joint attention (JA), which is the capacity to share Received 8 June 2018 attention on an object with another person. JA precedes the development of the capacity to Reviewed 10 September 2018 attribute mental states to others (i.e., mentalization or theory of mind). The neural Revised 30 October 2018 mechanisms involved in the development of mentalization are not fully understood. Accepted 17 December 2018 Electroencephalographic recordings were made of children while they watched stimuli on Action editor Kerstin Konrad a screen and their interaction with the experimenter was assessed. We tested whether Published online 2 January 2019 neuronal activity preceding JA correlates with mentalization in typically developing (TD) children and whether this activity is impaired in children with autistic spectrum disorder Keywords: (ASD) who evidence deficits in JA and mentalization skills. Both groups exhibited JA Childhood behavior with comparable frequency. TD children displayed a higher amplitude of negative EEG central (Nc) event-related potential preceding JA behavior (~500 msec after stimuli Neurodevelopmental disorders presentation), than did the ASD group. Previous to JA behavior, TD children demonstrated Temporoparietal junction beta oscillatory activity in the temporoparietal region, while ASD children did not show an Theory of mind increase in beta activity. In both groups, the beta power correlated with mentalization, suggesting that this specific neuronal mechanism is involved in mentalization, which used during social interaction. © 2018 Elsevier Ltd. All rights reserved. * Corresponding author. Laboratorio de Neurociencias Cognitivas, Departamento de Psiquiatrı´a, Facultad de Medicina, Pontificia Uni- versidad Catolica de Chile, Marcoleta 391, Santiago, 8330024, Chile. ** Corresponding author. Division de Neurociencias, Centro de Investigacion en Complejidad Social (neuroCICS), Facultad de Gobierno, Universidad del Desarrollo, Av. Las Condes 12461, Las Condes, Santiago, 7590943, Chile. E-mail addresses: [email protected] (P. Soto-Icaza), [email protected] (P. Billeke). https://doi.org/10.1016/j.cortex.2018.12.018 0010-9452/© 2018 Elsevier Ltd. All rights reserved. cortex 113 (2019) 210e228 211 2003). Several studies have shown a strong association 1. Introduction between Nc amplitude and recognition processing (De Haan, Johnson, & Halit, 2007; Luyster, Powell, Tager-Flusberg, & The extremely complex social functioning of adults arises from Nelson, 2014; Nelson & McCleery, 2008; Webb, Long, Nelson & several early onset behaviors that are the building blocks for Webb, 2005). The Nc seems to be generated in frontal cortical social behavior. One of these social precursors is the capacity to areas, such as the anterior cingulate cortex (ACC) and the share attention on an object with another person. This is called inferior frontal gyrus (IFG) (Richards et al., 2010). Additionally, joint attention (JA) (Charman et al., 2000; Happe & Frith, 2014; using oscillatory activity measures by EEG and metabolic Soto-Icaza, Aboitiz, & Billeke, 2015). JA can be responding or activity by near-infrared spectroscopy (NIRS), other studies initiating (Mundy & Jarrold, 2010). The former refers to the have demonstrated a crucial participation of lateral frontal ability to follow the direction of the gaze and gestures of others and lateral parietal regions during JA in infants (Grossmann & in order to share a common point of reference; the latter refers Johnson, 2010; Grossmann, Johnson, Farroni, & Csibra, 2007; to the ability to spontaneously point, show and use eye contact Ku¨ hn-Popp, Kristen, Paulus, Meinhardt, & Sodian, 2016; to share the experience of an object. While evidence shows that Mundy et al., 2000). responding JA emerges at around 6e9monthsofage The other line of evidence associates JA with the mentali- (Butterworth & Cochran, 1980; Kopp & Lindenberger, 2011; zation network in both adults and children that pass false Morgan, Maybery, & Durkin, 2003; Striano, Reid, & Hoehl, belief tests (the main marker of mentalization or theory of 2006), initiating JA does not appear until around the end of mind; Soto-Icaza et al., 2015). The mentalization network the first year of life/beginning of the second year of life (Mundy, consists of several cortical areas that show consistent activa- 2017). While it is agreed that responding JA encompasses a vi- tion when people figure out other people's intentions. In sual readjustment of a child's gaze in accordance with the typical adults, this network involves the temporoparietal change in the focus of visual attention of an adult (Butterworth junction (TPJ), the posterior superior temporal sulcus (pSTS), & Jarrett, 1991), there is no consensus on whether initiating JA the dorsomedial prefrontal cortex (dmPFC), the precuneus, the involves a child's understanding of other's intentions and temporal pole, and the inferior frontal gyrus (Schurz, Radua, thoughts (Moore, 1994). In spite of this controversy, it is well- Aichhorn, Richlan, & Perner, 2014). Neuroimaging research in known that JA plays a key role in social development, since it children, adolescents and adults shows that JA activates a results in a coordinated social behavior where the child shares brain network that overlaps with the mentalization network, a common experience with his/her partner without obtaining particularly in the TPJ, STS (Oberwelland et al., 2017) and something from him/her (Mundy, Card, & Fox, 2000), revealing dmPFC (Caruana, Brock & Woolgar, 2015; Oberwelland et al., its reciprocity quality (Oberwelland et al., 2017). Moreover, 2016; Redcay et al., 2010; Saito et al., 2010; Schilbach et al., several studies have shown that JA ability precedes the devel- 2010). It has been proposed that practicing JA provides a opment of the capacity to attribute mental states to others, that unique brainebehavior experience that is necessary for is, mentalization (Happe & Frith, 2014; Krall et al., 2016; Mundy sculpting the components of the neural systems for mentali- et al., 2000; Soto-Icaza et al., 2015). zation (Mundy, 2017; Mundy, Sullivan, & Mastergeorge, 2009). Studies of neurobiological JA mechanisms have provided A candidate structure for developing mentalization from JA two main lines of evidence. One is that JA is related to brain is the TPJ. Comparing JA studies between infants and children, activity associated with attention control in typically devel- TPJ becomes specifically activated in children with mentali- oping (TD) infants, which involves the dorsal attentional zation capacity (Mundy, 2017). In healthy adults and adoles- network and the fronto-parietal network (Eggebrecht et al., cents this area (especially the posterior segment involving the 2017; Mundy, 2017). These networks include lateral parietal angular gyrus; Igelstrom,€ Webb, Kelly, & Graziano, 2016; Lee & areas (the intraparietal sulcus, IPS) and lateral frontal areas McCarthy, 2016) is a key node of the network that participates (dorsolateral prefrontal cortex and frontal eye fields, FEF; in attributing mental states to others and perceiving the per- Eggebrecht et al., 2017; Power et al., 2011). During JA, these spectives and preferences of others during social interactions networks probably participate in the cognitive control related (Oberwelland et al., 2016; Van Overwalle, 2009). Indeed, using to exterocentive processing and contribute to maintain the non-invasive brain stimulation, recent studies have demon- attentional focus. Specifically, studies have demonstrated that strated the causal role of the TPJ in mentalization processes responses to JA modulate the negative central (Nc) component (Donaldson, Kirkovski, Rinehart, & Enticott, 2017; Hill et al., (Kopp & Lindenberger, 2011; Striano et al., 2006), which refers 2017). Additionally, the TPJ (probably the anterior segment to a negative deflection in frontocentral electrodes. It is involving the supramarginal gyrus (Igelstrom€ et al., 2016; Lee thought that the Nc reflects the reorientation of the attention & McCarthy, 2016)) is also part of the right-lateralized to salient stimuli (Richards, Reynolds, & Courage, 2010; Striano ventral attentional network related to detecting task- et al., 2006). Increases in the amplitude of this component have relevant stimuli and reorienting attentional responses been interpreted as attention activation (arousal), elicited by (Chang et al., 2013; Corbetta, Patel, & Shulman, 2008; an environmental stimulus (Soto-Icaza et al., 2015; Striano & Zamorano et al., 2017). Developmental changes in the func- Reid, 2006). Increases in arousal influence subsequent cogni- tion of this cortical area could underlie the emergence of tive processes like memory and learning (Hirotani,